new avian filarioids (nematoda: splendidofilariinae ...at nerve ring 100, 100, 90 ^m, at anus 50,...

Proc. Helminthol. Soc. Wash.54(1), 1987, pp. 1-14

New Avian Filarioids (Nematoda: Splendidofilariinae):Dessetfilaria guianensis gen. n., sp. n.,Andersonfilaria africanus gen. n., sp. n., andSplendidofilaria chandenieri sp. n.

CHERYL M. BARTLETT' AND ODILE BAIN2

1 Department of Zoology, College of Biological Science, University of Guelph,Guelph, Ontario NIG 2W1, Canada and2 Laboratoire des Vers, associe au CNRS, Museum National d'Histoire Naturelle,61 rue de Buffon, 75231 Paris Cedex 05, France

ABSTRACT: The following new taxa are described: Dessetfilaria guianensis gen. n., sp. n. from a capsule alongthe outer wall of the aorta in a channel-billed toucan (Ramphastos vitellinus Lichtenstein [Ramphastidae])collected near Cayenne, French Guiana; Andersonfilaria africanus gen. n., sp. n. from a fossa in the pelvic girdleof a common waxbill (Estrilda astrild (L.) [Estrildidae]) imported into France from Africa; and Splendidofilariachandenieri sp. n. from subcutaneous tissues of the wing of the same common waxbill. Microfilariae occurredin the blood. Dessetfilaria is characterized by the presence of only two pairs of cephalic papillae and a distinctlydivided esophagus. Chandlerella braziliensis Yeh, 1957, is transferred to Dessetfilaria as D. braziliensis (Yeh,1957) comb. n. Andersonfilaria is characterized by the presence of four pairs of cephalic papillae and a poorlydeveloped, undivided esophagus. Splendidofilaria chandenieri is distinguished from other bossate species fromsubcutaneous tissues by the absence of large preanal papillae.

KEY WORDS: Filarioidea, Ramphastos vitellinus, Estrilda astrild, bird parasites, microfilariae, nematode tax-onomy, morphology, French Guiana, Africa, Paris, France.

The numerous reports of microfilariae in theblood of birds in the Neotropical and Ethiopianzoogeographic regions (Bennett et al., 1982) in-dicate that the resident avifauna is widely par-asitized by filarioid nematodes. Few of the fi-larioid species present have been identified,however, largely because the requisite adultworms are often not looked for or, due to theircryptic locations, are overlooked. The presentpaper describes two new genera and three newspecies on the basis of material from a channel-billed toucan (Ramphastos vitellinus) from FrenchGuiana and a common waxbill (Estrilda astrild)from Africa.

Materials and Methods

The channel-billed toucan was obtained through thecourtesy of Mr. Ferrere in the region of Cayenne, FrenchGuiana, on 11 March 1983 and the common waxbillwas obtained through the courtesy of Mr. JacquesChandenier, who had purchased the bird at a pet storein Paris, France, in October 1985 after it had beenimported from Africa. Both birds were examined foradult filarioids, and adults recovered were fixed in hot70% alcohol, transferred to 70% alcohol/5% glycerin,and studied in glycerin. En face views were also studiedin lactophenol. Transverse sections were prepared free-hand using a mounted razor blade. Microfilariae fromthe blood or from the vagina were studied, and thespecific techniques used accompany the descriptions

of the microfilariae (blood smears were fixed in ethanoiprior to staining).

Results

Dessetfilaria gen. n.

DIAGNOSIS: Spirurida, Filarioidea, Oncho-cercidae, Splendidofilariinae Chabaud and Cho-quet, 1953 (sensu Anderson and Bain, 1976).Cephalic extremity with 2 pairs of papillae. Cu-ticle transversely striated. Esophagus divided,anterior portion narrow and poorly developed,posterior portion broad and glandular. Posteriorextremity of body bluntly rounded in both sexes.Caudal papillae in 2 ventrolateral rows. Spiculessubequal. Vulva pre-esophageal. Microfilaria withrounded tail. Parasites of birds. Type species: D.guianensis sp. n.

Dessetfilaria guianensis sp. n.(Figs. 1-27, 72)

GENERAL: Long, slender nematodes. Bodywidth uniform over most of length, but taperinggradually toward bluntly rounded extremities.Cuticle thin, transverse striations delicate at bothends of body but becoming increasingly apparentand wider toward midbody. Cuticle in lateralfields slightly thicker than elsewhere (Figs. 10,17, 22, 23) and not striated. Hemizonid readily

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PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY

visible, slightly protuberant. Triangular outlineof underlying hypodermal tissue visible in enface view of female; not observed in male. Ce-phalic papillae tiny and difficul t to discern, lin-early arranged with 2 on either side of oral open-ing, inner 2 not protuberant, outer 2 slightlysalient (Figs. 8, 16). Amphids slightly salient.Oral opening tiny, laterally compressed, andlacking circumoral ring. Pre-esophageal ring ab-sent. Anterior extremity of esophagus not welldenned (Figs. 2a, 4, 15a). Esophageal divisiondistinct (Figs, la, 14), anterior portion devoid oftransverse muscle fibers and much narrower thanposterior glandular portion. Anterior portioncontinuing into glandular portion (Figs. 2a, 5,15a), but becoming increasingly obscure towardposterior end of esophagus (Figs. 2d, 15d). Glan-dular portion markedly granular and containingnumerous large nuclei (Figs. 2, 15). Cuticularlining of esophageal lumen distinct and frequent-ly plicate in anterior portion (Fig. 4), obscure inposterior portion. Junction of esophageal and in-testinal tissues distinct and oblique (Figs. 2e, 3,15d, 21); junction of esophageal and intestinallumens difficul t to discern (Figs. 20a, b). Phas-mids not observed.

MAL E (3 specimens, measurements of holo-type followed by paratypes): Length 29, 26, 23mm. Maximum width 180, 160, 160 /urn. Widthat nerve ring 100, 100, 90 ^m, at anus 50, 55,55 yum. Approximate number of transverse cu-ticular striations over 100 /urn at midbody 28,29, 29. Nerve ring 140, 140, 120 ,um from an-terior extremity. Length of anterior portion onlyof esophagus 200, 145, 140 /mi; length of glan-dular portion of esophagus 1.48, 0.85, 1.02 mm.Maximum width of anterior portion of esopha-gus 18, 25, 25 /an; maximum width of glandularportion of esophagus 75, 95, 95 /on. Caudal endin 2, 1.5, 1.5 coils. Spicules (Figs. 6, 7) dissimilar,uniformly cuticularized, left 94, 108, 102 yum long,right 82, 78, 80 /im long. Anus 80, 84, 85 /mifrom posterior extremity. Cuticular lips of anusthick (Fig. 9). Small semipedunculate pre-, ad-,and postanal papillae present in 2 rows on tail;asymmetric or symmetric in arrangement; 7 onleft side and 8 on right side in holotype (Figs.11, 12), 7 or 8 on either side in paratypes (Fig.13).

FEMALE (3 gravid specimens, measurements ofallotype followed by paratypes): Length 85, 82,78 mm. Maximum width 300, 250, 250 /tin.Width at nerve ring 130, 125, 120 /nm, at vulva

180, 170, 190 /mi, at anus 80, 80, 75 /on. Ap-proximate number of transverse cuticular stria-tions over 100 /um at midbody 14, 15, 15. Nervering 150, 125, 180 /mi from anterior extremity.Length of anterior portion only of esophagus 230,180, 280 /urn; length of glandular portion ofesophagus 1.28, 1.04, 1.35 mm. Maximum widthof anterior portion of esophagus 20, 25, 22 /on;maximum width of glandular portion of esoph-agus 85, 82, 95 urn. Vulva 400, 350, 500 /mifrom anterior extremity. Cuticular lips of vulvathin, slightly salient (Fig. 24). Body not swollenin vulvar region (Fig. 14). Vagina directed pos-teriorly from vulva, not convoluted, 1.5, 2.3, 1.5mm long. Didelphic and opisthodelphic. Utericonvoluted. Ovaries in posterior region of body.Anus visible as slightly salient delicate opening95, 105, 140 /mi from posterior extremity (Fig.26). Posterior extremity with two inconspicuouspapillae (Figs. 25, 26).

MICROFILARIA : Body short (Fig. 72) withtransversely striated cuticle. Anterior extremitybluntly rounded. Cephalic cuticular structures notobserved. Body width greatest at midbody, ta-pering slightly toward extremities, taper morepronounced in posterior region. Posterior ex-tremity bluntly rounded. Posteriormost nucleusrounded, present at tail extremity (Fig. 72). Sheathabsent. Small inner body visible in some speci-mens. Measurements (in micrometers) as fol-lows:

1) 10 specimens from hematein-stained thinblood smears: length (range followed by mean)37-62 (53); maximum width 6-7.

2) 3 specimens in which some fixed points werevisible, from hematein-stained thin bloodsmears: length 58, 57, 55; maximum width7, 6, 6; length of cephalic space 3, 3, 2; dis-tance from anterior extremity to beginning ofinner body 30, 31, 33; length of inner body5, 2, 3; distance from anterior extremity toanal vesicle 48, 47, 46.

3) 10 specimens from the anterior vagina of afemale worm: length (range followed by mean)46-60 (54); maximum width 4-5.

TYPE HOST: Channel-billed toucan, Ram-phastos vitellinus Lichtenstein (Piciformes:Ramphastidae).

LOCATION IN HOST: Adults in delicate capsulealong outer wall of aorta near junction with heart.Microfilariae in blood.

TYPE LOCALITY : Cayenne, French Guiana.

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OF WASHINGTON, VOLUME 54, NUMBER 1, JANUARY 1987

Figures 1-13. Dessetfilaria guianensis gen. n., sp. n. 6. Holotype: Figures 1, 2, 9, 11, 12. Paratypes: Figures3-8, 10, 13. 1. Anterior end showing anteriormost region (la) and esophageal-intestinal junction (Ib); lateralview (locations of Fig. 2b-d indicated). 2. Anterior end (2a), detail of esophagus (2b-d), and detail of esophageal-intestinal junction (2e); lateral view. 3. Detail of esophageal-intestinal junction; views in different (3a, b) ori-entations. 4. Anterior extremity; lateral view. 5. Anterior end; lateral view. 6, 7. Spicules, right and left, respec-tively; lateral view. 8. En face view. A = amphid. 9. Detail of anal region; left lateral view. 10. Partial (lOa)and whole (lOb) transverse sections of midbody. 11-13. Posterior end; ventral, lateral, and lateral views, respec-tively.



Figures 14-27. Dessetfilaria guianensis gen. n., sp. n. 9. Allotype: Figures 14,15, 24. Paratypes: Figures 16-23, 25-27. 14. Anterior end; lateral view (locations of Fig. 15b, c indicated). 15. Anterior extremity (15a), detailof esophagus (15b, c), and detail of esophageal-intestinal junction (15d); lateral view. 16. En face view. A =amphid. 17. Transverse section of body immediately anterior to nerve ring. 18,19. Transverse sections of glandularportion of esophagus; anterior and posterior regions, respectively. 20. Transverse sections of esophageal-intestinaljunction at anteriormost (20a) and posteriormost (20b) regions. 21. Detail of esophageal-intestinal junction, viewsin different (21a, b) orientations. 22. Partial transverse section of body at esophageal-intestinal junction. 23.



SPECIMENS: Museum National d'HistoireNaturelle, Paris, France (MNHN). Holotype ($),allotype (2), and paratypes (<5 and 2): MNHN No.42 ED. Microfilariae: MNHN Nos. N VII 31-33.

TAXONOMIC COMMENTS: Within Splendido-filariinae (sensu Anderson and Bain, 1976) mostgenera have four pairs of cephalic papillae. Des-setfilaria gen. n., Splendidofilaria Skrjabin, 1923,and Thamugadia Seurat, 1917, have only twopairs, as might the monotypic and inadequatelydescribed genera Pseudothamugadia Lopez-Neyra, 1956, and Onchocercella Yorke, 1931(sensu Anderson and Bain, 1976; not sensu So-nin, 1977). The papillae in Dessetfilaria andSplendidofilaria from birds differ from those inThamugadia and Pseudothamugadia from rep-tiles, being generally small and asymmetricallyarranged as opposed to large and symmetric; thesefour genera have smooth or transversely striatedcuticles. The papillae in Onchocercella frommammals are small, and the cuticle has fusiformthickenings. In addition, in Thamugadia andPseudothamugadia the entire esophagus is broad,whereas in Dessetfilaria and Splendidofilaria theanterior portion of the esophagus is narrow. Des-setfilaria has, however, a broad glandular pos-terior portion, whereas the entire esophagus inSplendidofilaria is devoid of glandular tissue(Anderson, 1961; Anderson and Bain, 1976) al-though occasionally abnormally dilated poste-riorly (Bartlett and Anderson, 1985). The esoph-agus in Dessetfilaria is distinctly demarcated fromthe intestine but this is generally not the case inSplendidofilaria.

ETYMOLOGY: Dessetfilaria gen. n. is namedin honor of Pierre Desset and Marie-Claude Du-rette-Desset of Paris, France; "guianensis" de-notes the country where the infected bird wascollected.

OTHER SPECIES: Chandlerella braziliensis Yeh,1957, from a red breasted (=green billed) toucan(Ramphastos dicolorus L.) that died in the gardenof the Zoological Society of London after havingbeen imported from Brazil, is herein transferredto Dessetfilaria as D. braziliensis (Yeh, 1957)comb, n., based on the close resemblance of thespicules, pattern of caudal papillae, and major

dimensions to D. guianensis. Yeh (1957) statedthat "the digestive tract is not very well defined,"but "the rather indistinct esophagus appears di-vided into muscular and glandular parts." Thislack of observable detail was probably due toautolysis, as the specimens had come from a birdthat had been dead for an unknown length oftime. Nevertheless, Yeh did clearly illustrate anarrow anterior portion in the esophagus and abroad posterior portion. He did not describe theen face view.

Dessetfilaria guianensis can be considered dis-tinct from D. braziliensis because the former isnarrower (160-180 vs. 200-250 /mi in males,250-300 vs. 380-460 jum in females) and has alonger glandular esophagus (850-1,480 vs. 500-540 Mm in males, 1,040-1,350 vs. 770-840 urnin females). Inadvertent flattening of the speci-mens and intraspecific variation might accountfor these "differences," but because the typespecimens of D. braziliensis are apparently lost(they are no longer present in the Helmintho-logical Collection of the London School of Hy-giene and Tropical Medicine [R. Muller, pers.comm.]), it seems best to consider the specimensfrom the channel-billed toucan as a new species(i.e., D. guianensis) and to base the descriptionof Dessetfilaria on this material. The status of D.braziliensis and D. guianensis requires furtherevaluation, however, especially in view of theclose ecologic and taxonomic relationship be-tween their hosts. Haffer (1974) considered chan-nel-billed and red-breasted toucans as a super-species, noting that they are parapatric except insoutheastern Brazil where they are locally sym-patric and that they occupy the lower strata inlowland Neotropical forests.

Andersonfilaria gen. n.

DIAGNOSIS: Spirurida, Filarioidea, Oncho-cercidae, Splendidofilariinae Chabaud and Cho-quet, 1953 (sensu Anderson and Bain, 1976).Cephalic extremity with 4 pairs of papillae. Cu-ticle transversely striated. Esophagus not divid-ed, poorly developed. Esophageal-intestinaljunction indistinct. Posterior extremity of bodybluntly rounded in both sexes. Caudal papillaetiny and few in number. Spicules subequal. Vul-

Partial (23a) and whole (23b) transverse sections of midbody. 24. Vulva and anterior vagina; lateral view. 25,26. Posterior extremity; ventral and lateral views, respectively. 27. Posterior end, lateral view.



200 ym

Figures 28-38. Andersonfilaria africanus gen. n., sp. n. <5, holotype. 28. Anterior end; lateral view. H =hemizonid. 29. Anterior extremity, dorsal-ventral view. 30, 31. Spicules, right and left, respectively; lateral view.32. Outline of body; lateral view. 33, 34. Posterior extremity; right and left lateral views, respectively. 35, 36.Anal region; left and right lateral views, respectively. E = exudate. 37, 38. Posterior end; lateral and ventralviews, respectively. E = exudate.

va near esophageal-intestinal junction. Micro-filaria with attenuated tail. Parasites of birds. Typespecies: A. africanus sp. n.

Andersonfilaria africanus sp. n.(Figs. 28-51, 73-75)

GENERAL: Short, slender nematodes. Bodywidth uniform over most of length but taperinggradually toward bluntly rounded extremities.Anterior end with constricted neck region andbulbous extremity. Cuticle thick, transverse

striations delicate and closely spaced. Cuticle inlateral fields slightly thicker than elsewhere (Fig.43) and not striated. Hemizonid readily visible,markedly protuberant in male and gravid female(Figs. 28, 39). Outline of underlying hypodermaltissue not observed in en face view of nongravidfemale (en face views of gravid female and malenot examined). Cephalic papillae readily appar-ent, salient, symmetrically arranged in 2 circles,inner papillae slightly larger than outer (Fig. 42).Amphids not salient. Oral opening tiny, laterally



Figures 39-51. Andersonfilaria africanus gen. n., sp. n. 9. Allotype: Figures 39-41, 45-50. Paratypes: Figures42-44,51.39. Anterior end; lateral view. H = hemizonid. 40. Vulva and anterior vagina; lateral view. 41. Anteriorextremity; lateral view. 42. En face view. A = amphid. 43. Whole (43a) and partial (43b) transverse sections ofmidbody. 44. Anterior end; lateral view. 45,46. Outlines of anterior and posterior ends, respectively; reproductivetract only shown. 47. Posterior end; lateral view. 48. Anal region, ventral view. 49-51. Posterior extremity;ventral, lateral, and lateral views, respectively.



compressed, with delicate circumoral ring. Pre-esophageal ring absent. Anterior extremity ofesophagus not well denned (Figs. 29, 41). Esoph-agus narrow in anterior region but increasingslightly in width posteriorly, neither muscularnor glandular tissue apparent (Figs. 28, 39), pos-terior region occasionally containing variable-sized vacuoles (Fig. 44). Cuticular lining ofesophageal lumen difficul t to discern. Gradualindistinct transition marking change from esoph-agus to intestine (Fig. 39). Phasmids subtermi-nal.

MALE (1 specimen, holotype): Length 2.1mm. Maximum width 85 pm. Width of head 35nun, at constriction in neck region 31 jum, at nervering 43 jum, at anus 42 /urn. Approximate numberof transverse cuticular striations over 100 ^m atmidbody 130. Nerve ring 104 jum from anteriorextremity. Approximate length of esophagus 210fj.m. Maximum width of esophagus 12 jum. Pos-terior end of body in loose C-shaped ventralcurve, not coiled or twisted. Spicules (Figs. 30,31) dissimilar, uniformly cuticularized, left 55/urn long, right 37 /im long. Anus 88 nm fromposterior extremity (note: a teardrop-shaped ex-udate extends posteriorly from the anal opening[Figs. 35, 36, 38]). Cuticular lips of anus thick,forming delicate circumanal ring (Fig. 38). Del-icate nervelike strand of tissue present imme-diately anterior to anus, extending from hypo-dermis to cuticular surface (Figs. 35, 36). One(?2) minute adanal papilla(e) present on right side(Figs. 36, 38). No adanal papillae visible on leftside (Fig. 35). Two small, sessile subterminalcaudal papillae present (Fig. 38).

FEMALE (3 specimens, measurements of gravidallotype followed by 2 nongravid paratypes [sec-ond paratype damaged]): Length 9.7, 7.8, 6.7mm. Maximum width 160, 114, 116 fJ-rn. Widthof head 40, 38, 38 /urn, at constriction in neckregion 35, 35, 36 /nm, at nerve ring 45, 50, —jim, at vulva 85, 80, 85 jum, at anus 58, 66, —jum. Approximate number of transverse cuticularstriations over 100 i*m at midbody 43, 56, 65.Nerve ring 110, 90, — ;um from anterior extrem-ity. Approximate length of esophagus 260, 280,360 /^m. Maximum width of esophagus 15, 18,12 /um. Vulva 290, 260, 265 i^m from anteriorextremity. Lips of vulva same thickness as bodycuticle, not protuberant (Fig. 40). Body swollenin vulvar region (Figs. 39, 45). Vagina directedposteriorly from vulva, occasionally looping,—, 930, 850 urn long. Didelphic and opisthodel-

phic. Uteri convoluted. Ovaries in posteriorquarter of body. Anus visible as slightly salientdelicate opening 188, 194, — ̂ m from posteriorextremity (Figs. 47, 48). Posterior extremity withslight bilateral swelling (Figs. 49-51).

MICROFILARIA : Body long (Fig. 74) withtransversely striated cuticle. Anterior extremitybluntly rounded. V-shaped, cephalic cuticularstructure present. Body width uniform over an-terior % of body, posterior region gradually ta-pering into attenuated tail with rounded extrem-ity. Posteriormost nuclei elongate and linearlyarranged, not extending to tail extremity (Fig.73). Striated sheath present; tight around wholeof body of microfilaria (Fig. 75) (note: sheathreadily visible in Giemsa-stained thin bloodsmears and generally having become detachedfrom body of microfilaria [Fig. 73], obscure inlive specimens [Fig. 75], not visible in hematein-stained thin blood smears). Small inner body vis-ible in some specimens. Measurements (in mi-crometers) as follows:

1) 10 specimens from each of 4 preparations,length (range with mean in parentheses) andmaximum width:a) wet preparation (i.e., cover glass placed

over drop of blood on slide), not stained(note: microfilariae were examined 24 hrafter the preparation was made and at thistime were moribund): 239-267 (255); 7.

b) Giemsa-stained thin blood smear: 196-225(209); 4.

c) Giemsa-stained thick blood smear: 198-245 (214); 4.

d) hematein-stained thin blood smear: 195-231 (213); 4-5.

2) 3 specimens in which some fixed points werevisible, from Giemsa-stained thin bloodsmear: length 190, 215, 225; excretory pore45, 45, 50; beginning of inner body 103, 118,125; anal pore 140, 160, 170.

TYPE HOST: Common waxbill, Estrilda as-trild (L.) (Passeriformes: Estrildidae).

LOCATION IN HOST: Adults within fossa indorsal wall of pelvic girdle underneath middleregion of right kidney. Microfilariae in blood.

TYPE LOCALITY: Africa. Note: the bird wasimported from Africa into Paris, France, whereit was purchased at a pet store. The commonwaxbill is native to most of Africa south of theSahara (Walters, 1980).

SPECIMENS: Museum National d'Histoire



l52a

K

5455

58

52 b

60 a

Figures 52-60. Splendidofilaria chandenieri sp. n. <5, holotype. 52. Anterior end, showing anteriormost region(52a) and esophageal-intestinal junction (52b); dorsal-ventral view. 53. Anterior extremity; dorsal-ventral view.54, 55. Cuticle; lateral and surface views, respectively. 56, 57. Spicules, right and left, respectively; lateral view.58, 59. Posterior end, lateral views. 60. Posterior end, showing anal region (60a) and extremity (60b); ventral


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Figures 61-71. Spendidofilaria chandenieri sp. n. 2, allotype. 61. Anterior end; lateral view. 62. Anteriorextremity; dorsal-ventral view. 63. En face view. A = amphid. 64. Esophageal-intestinal junction; lateral view.65. Partial transverse section of midbody. L = lateral field. 66-68. Cuticle; surface, lateral, and lateral views,respectively. 69. Vulva and anterior vagina; lateral view. 70. Posterior extremity; lateral view. 71. Posterior end;lateral view.

Naturelle, Paris, France (MNHN). Holotype (<3),allotype ($), and paratypes (9): MNHN No. 85DL. Microfilariae: MNHN Nos. N VII 28-30,42, 43.

TAXONOMIC COMMENTS: Within Splendidio-nlariinae, the four pairs of cephalic papillae andundivided, poorly developed esophagus in An-

dersonfilaria gen. n. from birds are also seen onlyin Micipsella Seurat, 1921, from lagomorphs andCardianema Alicata, 1933, from turtles. How-ever, Andersonfilaria and Micipsella have small,uniformly cuticularized spicules, whereas Car-dianema has rather long spicules, the distal partsof which are membranous. Andersonfilaria has a


OF WASHINGTON, VOLUME 54, NUMBER 1, JANUARY 1987 11

25 pirn

76

Figures 72-79. Microfilariae (striations on body and/or on sheath not illustrated). 72. Dessetfllaria gui-anensis gen. n., sp. n.; from hematein-stained thin blood smear. 73. Andersonfilaria africanus gen. n., sp. n.; fromGiemsa-stained thin blood smear; note sheath (S), which has detached from body of microfilaria. 74. Anderson-filaria africanus, outline of body; from unstained wet preparation. 75. Andersonfilaria africanus, detail of anteriorend, midbody, and posterior end; note tight sheath (S); from unstained wet preparation. 76. Splendidofilariachandenieri sp. n., outline of body; from unstained wet preparation. 77, 78. Splendidofilaria chandenieri, anteriorend, showing "pinched" appearance; from unstained wet preparation. 79. Splendidofilaria chandenieri, detail ofposterior end; from unstained wet preparation.

smooth cuticle, whereas Micipsella has a bossatecuticle; moreover, the minute size (2.1 mm) ofthe male of A. africanus clearly contrasts withthe large size (22-100 mm) of the males of Mi-cipsella species. The long microfilaria with anattenuated tail and the reduced number of caudalpapillae in Andersonfilaria are reminiscent ofCardiqfilaria Strom, 1937, from birds. Ander-sonfilaria has, however, a poorly developedesophagus that is indistinctly demarcated fromthe intestine, whereas Cardiofilaria has a broadmuscular esophagus, clearly demarcated from theintestine. Cardiofilaria also has a pre-esophagealring, which Andersonfilaria lacks.

ETYMOLOGY: Andersonfilaria gen. n. is namedin honor of Professor Roy C. Anderson of Guelph,Ontario, Canada; "africanus'" denotes the con-tinent from which the infected bird was import-ed.

Splendidofilaria chandenieri sp. n.(Figs. 52-71, 76-79)

GENERAL: Spirurida, Filarioidea, Onchocer-cidae, Splendidofilariinae Chabaud and Cho-quet, 1953 (sensu Anderson and Bain, 1976),Splendidofilaria Skjrabin, 1923 (sensu Andersonand Bain, 1976). Long, slender nematodes. Bodywidth uniform over most of length, but tapering


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gradually toward bluntly rounded extremities.Cuticle thin, transversely striated, with variable-sized oval to round bosses (Figs. 54, 55, 65-68).Bosses generally single, rarely double, not ex-tending to extremities of body and not arrangedin any discernible pattern; each boss with a round,more dense central portion. Cuticle in lateral fieldsnot thicker than elsewhere (Fig. 65), striated. Ovaloutline of underlying hypodermal tissue visiblein en face view of female (en face view of malenot examined). Cephalic papillae readily appar-ent, asymmetrically arranged in broad circlearound oral opening (Fig. 63). Amphids slightlysalient. Oral opening tiny, laterally compressed,with delicate circumoral ring. Pre-esophageal ringabsent. Anterior extremity of esophagus not welldefined (Figs. 53, 62). Esophagus narrow, devoidof glandular tissue (Figs. 52, 61), posterior halfwith numerous large nuclei (Fig. 64). Cuticularlining of esophageal lumen difficul t to discern.Junction of esophagus and intestine not well de-fined (Fig. 64). Caudal languettes not present.Phasmids terminal.

MALE (1 specimen, holotype): Length 17 mm.Maximum width 65 yum. Width of body at nervering 32 /um, at anus 42 /um. Number of transversecuticular striations over 100 /urn at midbody 90.Bosses commencing approximately l/2 mm fromanterior extremity, ending approximately 1 mmanterior to anus. Nerve ring 105 /urn from an-terior extremity. Approximate length of esoph-agus 545 jum. Maximum width of esophagus 9jttm. Posterior end of body in loose C-shapedventral curve, not coiled or twisted. Spicules (Figs.56, 57) slightly dissimilar, uniformly cuticular-ized, both 45 jum long. Anus 110 /j,m from pos-terior extremity. Cuticular lips of anus thickestposteriorly. Hypodermal swelling present im-mediately anterior to and posterior to anus (Fig.60a). Preanal papillae absent. Sessile adanal pa-pillae present, consisting of 2 obscure papillae atbase of anterior hypodermal swelling and 2 largerpapillae lateral to posterior hypodermal swelling(Fig. 60a). Semipedunculate postanal papillaepresent, consisting of 2 pairs on posterior half oftail (Figs. 58, 59, 60b).

FEMALE (1 gravid specimen, allotype): Length38 mm. Maximum width 140 /urn. Width at nervering 50 yum, at vulva 72 /urn, at anus 45 /urn.Number of transverse cuticular striations over100 Mm at midbody 75. Bosses commencingslightly posterior to vulva, ending approximately130 Atm anterior to anus. Nerve ring 110 fj.m from

anterior extremity. Approximate length ofesophagus 565 ^m. Maximum width of esoph-agus 10 pm. Vulva 385 fim from anterior ex-tremity. Cuticular lips of vulva thick, slightlysalient (Fig. 69). Body not swollen in vulvar re-gion (Fig. 61). Vagina directed posteriorly fromvulva, not convoluted, 1.3 mm long. Didelphicand opisthodelphic. Ovaries in posterior 3 mmof body. Anus visible as salient, readily apparentopening 150 jum from posterior extremity (Fig.71).

MICROFILARIA: Body short (Fig. 76) withtransversely striated cuticle. Anterior extremitybluntly rounded, appearing "pinched" in somespecimens (Figs. 77, 78). Two minute, cephaliccuticular structures present. Body width uniformover anterior % of body, posterior region taperingslightly toward rounded extremity. Posterior-most nucleus rounded, present at tail extremity(Fig. 79). Sheath absent. Small inner body pres-ent. Measurements (in micrometers) as follows:

1) 10 specimens from each of 4 preparations,length (range with mean in parentheses) andmaximum width:a) Wet preparation (i.e., cover glass placed

over drop of blood on slide), not stained(note: the microfilariae were examined 24hr after the preparation was made and atthis time were moribund): 96-113 (106);4-6.

b) Giemsa-stained thin blood smear: 47-68(58); 3-4.

c) Giemsa-stained thick blood smear: 45-75(59); 3-4.

d) hematein-stained thin blood smear: 43-50(47); 3-4.

TYPE HOST: Common waxbill, Estrilda as-trild (L.) (Passeriformes: Estrildidae).

LOCATION IN HOST: Adults in subcutaneousconnective tissue near distal end of right hu-merus. Microfilariae in blood.

TYPE LOCALITY: Africa. Note: the bird wasimported from Africa into Paris, France, whereit was purchased at a pet store. The commonwaxbill is native to most of Africa south of theSahara (Walters, 1980).

SPECIMENS: Museum National d'HistoireNaturelle, Paris, France (MNHN). Holotype (3)and allotype ($): MNHN No. 85 DL. Microfi-lariae: MNHN Nos. N VII 28-30, 42, 43.

TAXONOMI C COMMENTS: Sixteen bossatespecies of Splendidofilaria have been previously


OF WASHINGTON, VOLUME 54, NUMBER 1, JANUARY 1987 13

described, 11 from the heart or body cavity ofthe host and five from the subcutaneous tissues.Splendidofilaria chandenieri sp. n. can be distin-guished easily from other subcutaneous species,as S. gedoelsti Travassos, 1926, S. gvozdevi So-nin and Barus, 1978, S. singhi Sultana, 1962, S.columbensis Olsen and Braun, 1976, and S. hib-leri Olsen and Braun, 1976, have large preanalpapillae, which are lacking in the new species.

ETYMOLOGY: The new species is named inhonor of Mr. Jacques Chandenier of Paris,France.

Discussion

Significant progress has been made in avianfilarioid systematics in the past 25 yr, yet, be-cause of our limited knowledge of the filarioidfauna of birds in the equatorial regions and theSouthern Hemisphere, undescribed taxa likelyremain. The present study, in describing two newgenera and three new species, places significantgeneric value on esophageal morphology andnumber of cephalic papillae, and thus followsearlier proposals by Anderson (1961, 1968) andAnderson and Bain (1976).

The poorly developed, undivided esophagusin Splendidofilaria and Anderson/Maria likelyevolved from a well-developed, either dividedor undivided, esophagus as in the presumed spi-rurid ancestors of the filarioids and in numerousextant filarioid genera. The esophagus in Des-setfilaria guianensis has no apparent musculartissue in the reduced anterior portion, and thusmay represent an intermediate stage in this evo-lution. The poorly developed, undivided esoph-agus appears to have arisen independently on anumber of occasions, however, as it occurs inOnchocercinae and Lemdaninae as well as inSplendidofilariinae.

Anderson (1968) suggested that the cephalicpapillae pattern observed in Pseudofilaria Sand-ground, 1935 (four submedian pairs plus six pa-pillae in an inner circle), be regarded as the mostprimitive filarioid type, and he outlined the mor-phologic changes by which the "typical filarioidpattern" of only four submedian pairs (such asthat in Andersonfilaria and the majority of gen-era) could be attained and eventually give rise tothe highly specialized condition of only two, oftenasymmetric, pairs in Splendidofilaria. The ex-treme reduction in size and the linear arrange-ment of the two pairs in Dessetfilaria appears to

be a further specialization of the Splendidofilariacondition.

The new taxa described in the present studywere found in birds of the families Ramphastidaeand Estrildidae. The former family is indigenousto the tropics of the New World, and 33 speciesare recognized, most being restricted to lowlandforests, although there are a few exceptions (Haf-fer, 1974). Ramphastids are semigregarious, es-pecially when feeding, and nest in tree cavities.In addition to Dessetfilaria guianensis and D.braziliensis, filarioids reported from the familyinclude Eulimdana micropenis (Travassos, 1926)Bartlett, Wong, and Anderson, 1985, Splendi-dofilaria gedoelsti Travassos, 1926, and Pelecitushelidnus (Molin, 1860) Railliet and Henry, 1910.

The family Estrildidae (sometimes considereda subfamily of Ploceidae) contains about 125species occurring in Africa, southeast Asia, andAustralia (Walters, 1980). In general, estrildidsoccur in grasslands, scrublands, forest edges, for-ests, and clearings. A few occur in marshes. Theyare highly gregarious and many nest in huge col-onies consisting of large domed nests. In additionto Andersonfilaria africanus and Splendidofilariachandenieri, filarioids reported from Estrildidaeinclude Chandlerella sultana (Sonin, 1966) An-derson and Freeman, 1969, and Eufilaria mcin-toshi Anderson and Bennett, 1960.

Acknowledgments

We thank Mr. Ferrere of Cayenne, FrenchGuiana, and Mr. Chandenier of Paris, France,who provided the infected birds. This study wassupported by the Museum National d'HistoireNaturelle, Paris, France. C. M. Bartlett was therecipient of a Postdoctoral Fellowship from theNatural Sciences and Engineering ResearchCouncil of Canada.

Literature Cited

Anderson, R. C. 1961. Splendidofilaria wehri n. sp.with a revision of Splendidofilaria and relatedspecies. Canadian Journal of Zoology 39:201-207.

. 1968. The comparative morphology of ce-phalic structures in the superfamily Filarioidea(Nematoda). Canadian Journal of Zoology 46:181-199.

, and O. Bain. 1976. Keys to the genera of theorder Spirurida. Part 3. Diplotriaenoidea, Aproc-toidea, and Filarioidea. Pages 59-116 in R. C.Anderson, A. G. Chabaud, and S. Willmott, eds.CIH Keys to the Nematode Parasites of Verte-brates. No. 3. Commonwealth Agricultural Bur-eaux, Farnham Royal, Buckinghamshire, England.


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Bartlett, C. M., and R. C. Anderson. 1985. On thefilarioi d nematodes from the pulmonary arteriesof birds. Canadian Journal of Zoology 63:2373-2377.

Bennett, G. F., M. Whiteway, and C. Woodworth-Ly-nas. 1982. A host-parasite catalogue of the avianhaematozoa. Memorial University of Newfound-land, Occasional Papers in Biology, No. 5.

Haffer, J. 1974. Avian speciation in tropical SouthAmerica. With a systematic survey of the toucans(Ramphastidae) and jacamars (Galbulidae). Pub-lication of the Nuttall Ornithological Club, No.14.

Sonin, M. D. 1977. Filariata of animals and man and

diseases caused by them. In K. M. Ryzhikov, ed.Fundamentals of Nematology. Vol. 28, Part 4. Iz-datel'stvo "Nauka," Moscow, U.S.S.R. (Translat-ed from Russian for the United States Departmentof Agriculture by Amerind Publishing Co. Pvt.Ltd., 66 Janpath, New Delhi 110001, India, 1985.)

Walters, M. 1980. The Complete Birds of the World.David & Charles (Publishers) Limited, NewtonAbbot.

Yeh, L. S. 1957. On Chandlerella braziliensis n. sp.from a green-billed toucan and a discussion onsome related genera. Journal of Helminthology 31:33-38.


new avian filarioids (nematoda: splendidofilariinae ...at nerve ring 100, 100, 90 ^m, at anus 50,...

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